Abstract
Sake yeast strains belonging to the budding yeast Saccharomyces cerevisiae exhibit higher rates of alcoholic fermentation and ethanol yields in the sake mash than the other types of S. cerevsiae strains. Although this has traditionally been regarded to be caused by their higher resistance against ethanol and various environmental stresses, recent studies revealed that they are rather defective in stress responses. Our genomic and transcriptomic approaches has led to the identification of the sake yeast-specific loss-of-function mutations in the MSN4, PPT1, and RIM15 genes, each of which has important roles in the responses to environmental changes. Surprisingly, each of these mutations contributes to the increase of alcoholic fermentation rate. Thus, we first reported the causal mutations for the high alcoholic fermentation ability of industrial yeast strains. These findings have drastically changed how we understand the relationship between ethanol tolerance and ethanol production ability of yeast cells. In this review, we introduce the history and progression of sake yeast studies, especially focusing on their superior alcoholic fermentation properties.
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References
Akao T, Yashiro I, Hosoyama A, Kitagaki H, Horikawa H, Watanabe D, Akada R, Ando Y, Harashima S, Inoue T, Inoue Y, Kajiwara S, Kitamoto K, Kitamoto N, Kobayashi O, Kuhara S, Masubuchi T, Mizoguchi H, Nakao Y, Nakazato A, Namise M, Oba T, Ogata T, Ohta A, Sato M, Shibasaki S, Takatsume Y, Tanimoto S, Tsuboi H, Nishimura A, Yoda K, Ishikawa T, Iwashita K, Fujita N, Shimoi H (2011) Whole-genome sequencing of sake yeast Saccharomyces cerevisiae Kyokai no. 7. DNA Res 18:423–434
Alper H, Moxley J, Nevoigt E, Fink GR, Stephanopoulos G (2006) Engineering yeast transcription machinery for improved ethanol tolerance and production. Science 314:1565–1568
Amorós M, Estruch F (2001) Hsf1p and Msn2/4p cooperate in the expression of Saccharomyces cerevisiae genes HSP26 and HSP104 in a gene- and stress type-dependent manner. Mol Microbiol 39:1523–1532
Aranda A, Querol A, del Olmo ML (2002) Correlation between acetaldehyde and ethanol resistance and expression of HSP genes in yeast strains isolated during the biological aging of sherry wines. Arch Microbiol 177(4):304–312
Azumi M, Goto-Yamamoto N (2001) AFLP analysis of type strains and laboratory and industrial strains of Saccharomyces sensu stricto and its application to phenetic clustering. Yeast 18:1145–1154
Bessonov K, Walkey CJ, Shelp BJ, van Vuuren HJ, Chiu D, van der Merwe G (2013) Functional analyses of NSF1 in wine yeast using interconnected correlation clustering and molecular analyses. PLoS One 8:e77192
Bleoanca I, Silva AR, Pimentel C, Rodrigues-Pousada C, Menezes Rde A (2013) Relationship between ethanol and oxidative stress in laboratory and brewing yeast strains. J Biosci Bioeng 116:697–705
Blieck L, Toye G, Dumortier F, Verstrepen KJ, Delvaux FR, Thevelein JM, Van Dijck P (2007) Isolation and characterization of brewer’s yeast variants with improved fermentation performance under high-gravity conditions. Appl Environ Microbiol 73:815–824
Boorsma A, Foat BC, Vis D, Klis F, Bussemaker HJ (2005) T-profiler: scoring the activity of predefined groups of genes using gene expression data. Nucleic Acids Res 33((Web Server Issue)):W592–W595
Borneman AR, Desany BA, Riches D, Affourtit JP, Forgan AH, Pretorius IS, Egholm M, Chambers PJ (2011) Whole-genome comparison reveals novel genetic elements that characterize the genome of industrial strains of Saccharomyces cerevisiae. PLoS Genet 7:e1001287
Cameroni E, Hulo N, Roosen J, Winderickx J, De Virgilio C (2004) The novel yeast PAS kinase Rim15 orchestrates G0-associated antioxidant defense mechanisms. Cell Cycle 3:462–468
Casey GP, Ingledew WM (1986) Ethanol tolerance in yeasts. Crit Rev Microbiol 13:219–280
Causton HC, Ren B, Koh SS, Harbison CT, Kanin E, Jennings EG, Lee TI, True HL, Lander ES, Young RA (2001) Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell 12:323–337
D’Amore T, Stewart GG (1987) Ethanol tolerance of yeast. Enzyme Microb Technol 9:322–330
Eastmond DL, Nelson HC (2006) Genome-wide analysis reveals new roles for the activation domains of the Saccharomyces cerevisiae heat shock transcription factor (Hsf1) during the transient heat shock response. J Biol Chem 281:32909–32921
Estruch F, Carlson M (1993) Two homologous zinc finger genes identified by multicopy suppression in a SNF1 protein kinase mutant of Saccharomyces cerevisiae. Mol Cell Biol 13:3872–3881
Ferguson SB, Anderson ES, Harshaw RB, Thate T, Craig NL, Nelson HC (2005) Protein kinase A regulates constitutive expression of small heat-shock genes in an Msn2/4p-independent and Hsf1p-dependent manner in Saccharomyces cerevisiae. Genetics 169:1203–1214
Furukawa K, Kitano H, Mizoguchi H, Hara S (2004) Effect of cellular inositol content on ethanol tolerance of Saccharomyces cerevisiae in sake brewing. J Biosci Bioeng 98:107–113
Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11:4241–4257
Gibson BR, Boulton CA, Box WG, Graham NS, Lawrence SJ, Linforth RS, Smart KA (2008) Carbohydrate utilization and the lager yeast transcriptome during brewery fermentation. Yeast 25:549–562
Görner W, Durchschlag E, Martinez-Pastor MT, Estruch F, Ammerer G, Hamilton B, Ruis H, Schüller C (1998) Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Genes Dev 12:586–597
Hahn JS, Thiele DJ (2004) Activation of the Saccharomyces cerevisiae heat shock transcription factor under glucose starvation conditions by Snf1 protein kinase. J Biol Chem 279:5169–5176
Hahn JS, Hu Z, Thiele DJ, Iyer VR (2004) Genome-wide analysis of the biology of stress responses through heat shock transcription factor. Mol Cell Biol 24:5249–5256
Hayashida S, Feng D, Hongo M (1974) Function of the high concentration alcohol-producing factor. Agric Biol Chem 38:2001–2006
Hong ME, Lee KS, Yu BJ, Sung YJ, Park SM, Koo HM, Kweon DH, Park JC, Jin YS (2010) Identification of gene targets eliciting improved alcohol tolerance in Saccharomyces cerevisiae through inverse metabolic engineering. J Biotechnol 149:52–59
Huuskonen A, Markkula T, Vidgren V, Lima L, Mulder L, Geurts W, Walsh M, Londesborough J (2010) Selection from industrial lager yeast strains of variants with improved fermentation performance in very-high-gravity worts. Appl Environ Microbiol 76:1563–1573
Imazu H, Sakurai H (2005) Saccharomyces cerevisiae heat shock transcription factor regulates cell wall remodeling in response to heat shock. Eukaryot Cell 4:1050–1056
Inai T, Watanabe D, Zhou Y, Fukada R, Akao T, Shima J, Takagi H, Shimoi H (2013) Rim15p-mediated regulation of sucrose utilization during molasses fermentation using Saccharomyces cerevisiae strain PE-2. J Biosci Bioeng 116:591–594
Ivorra C, Pérez-OrtÃn JE, del Olmo M (1999) An inverse correlation between stress resistance and stuck fermentations in wine yeasts. A molecular study. Biotechnol Bioeng 64:698–708
Jakobsen BK, Pelham HR (1988) Constitutive binding of yeast heat shock factor to DNA in vivo. Mol Cell Biol 8:5040–5042
Kitagaki H, Shimoi H (2007) Mitochondrial dynamics of yeast during sake brewing. J Biosci Bioeng 104:227–230
Kitagaki H, Takagi H (2014) Mitochondrial metabolism and stress response of yeast: applications in fermentation technologies. J Biosci Bioeng 117:383–393
Lee P, Kim MS, Paik SM, Choi SH, Cho BR, Hahn JS (2013) Rim15-dependent activation of Hsf1 and Msn2/4 transcription factors by direct phosphorylation in Saccharomyces cerevisiae. FEBS Lett 587:3648–3655
Liti G, Carter DM, Moses AM, Warringer J, Parts L, James SA, Davey RP, Roberts IN, Burt A, Koufopanou V, Tsai IJ, Bergman CM, Bensasson D, O’Kelly MJ, van Oudenaarden A, Barton DB, Bailes E, Nguyen AN, Jones M, Quail MA, Goodhead I, Sims S, Smith F, Blomberg A, Durbin R, Louis EJ (2009) Population genomics of domestic and wild yeasts. Nature 458:337–341
Liu XD, Thiele DJ (1996) Oxidative stress induced heat shock factor phosphorylation and HSF-dependent activation of yeast metallothionein gene transcription. Genes Dev 10:592–603
Luo X, Talarek N, De Virgilio C (2011) Initiation of the yeast G0 program requires Igo1 and Igo2, which antagonize activation of decapping of specific nutrient-regulated mRNAs. RNA Biol 8:14–17
Ma M, Liu LZ (2010) Quantitative transcription dynamic analysis reveals candidate genes and key regulators for ethanol tolerance in Saccharomyces cerevisiae. BMC Microbiol 10:169
Marks VD, Ho Sui SJ, Erasmus D, van der Merwe GK, Brumm J, Wasserman WW, Bryan J, van Vuuren HJ (2008) Dynamics of the yeast transcriptome during wine fermentation reveals a novel fermentation stress response. FEMS Yeast Res 8:35–52
MartÃnez-Pastor MT, Marchler G, Schüller C, Marchler-Bauer A, Ruis H, Estruch F (1996) The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J 15:2227–2235
Mendes-Ferreira A, del Olmo M, GarcÃa-MartÃnez J, Jiménez-Martà E, Mendes-Faia A, Pérez-OrtÃn JE, Leão C (2007) Transcriptional response of Saccharomyces cerevisiae to different nitrogen concentrations during alcoholic fermentation. Appl Environ Microbiol 73:3049–3060
Mortimer RK, Johnston JR (1986) Genealogy of principal strains of the yeast genetic stock center. Genetics 113:35–43
Noguchi C, Watanabe D, Zhou Y, Akao T, Shimoi H (2012) Association of constitutive hyperphosphorylation of Hsf1p with a defective ethanol stress response in Saccharomyces cerevisiae sake yeast strains. Appl Environ Microbiol 78:385–392
Nozawa M, Takahashi T, Hara S, Mizoguchi H (2002) A role of Saccharomyces cerevisiae fatty acid activation protein 4 in palmitoyl-CoA pool for growth in the presence of ethanol. J Biosci Bioeng 93:288–295
Ogawa Y, Nitta A, Uchiyama H, Imamura T, Shimoi H, Ito K (2000) Tolerance mechanism of the ethanol-tolerant mutant of sake yeast. J Biosci Bioeng 90:313–320
Olesen K, Felding T, Gjermansen C, Hansen J (2002) The dynamics of the Saccharomyces carlsbergensis brewing yeast transcriptome during a production-scale lager beer fermentation. FEMS Yeast Res 2:563–573
Pedruzzi I, Dubouloz F, Cameroni E, Wanke V, Roosen J, Winderickx J, De Virgilio C (2003) TOR and PKA signaling pathways converge on the protein kinase Rim15 to control entry into G0. Mol Cell 12:1607–1613
Pereira FB, Guimarães PM, Gomes DG, Mira NP, Teixeira MC, Sá-Correia I, Domingues L (2011) Identification of candidate genes for yeast engineering to improve bioethanol production in very high gravity and lignocellulosic biomass industrial fermentations. Biotechnol Biofuels 4:57
Rossignol T, Dulau L, Julien A, Blondin B (2003) Genome-wide monitoring of wine yeast gene expression during alcoholic fermentation. Yeast 20:1369–1385
Rossouw D, Bauer FF (2009) Comparing the transcriptomes of wine yeast strains: toward understanding the interaction between environment and transcriptome during fermentation. Appl Microbiol Biotechnol 84:937–954
Rossouw D, van den Dool AH, Jacobson D, Bauer FF (2010) Comparative transcriptomic and proteomic profiling of industrial wine yeast strains. Appl Environ Microbiol 76:3911–3923
Santos J, Sousa MJ, Cardoso H, Inácio J, Silva S, Spencer-Martins I, Leão C (2008) Ethanol tolerance of sugar transport, and the rectification of stuck wine fermentations. Microbiology 154:422–430
Sasano Y, Watanabe D, Ukibe K, Inai T, Ohtsu I, Shimoi H, Takagi H (2012) Overexpression of the yeast transcription activator Msn2 confers furfural resistance and increases the initial fermentation rate in ethanol production. J Biosci Bioeng 113:451–455
Schmitt AP, McEntee K (1996) Msn2p, a zinc finger DNA-binding protein, is the transcriptional activator of the multistress response in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 93:5777–5782
Shahsavarani H, Sugiyama M, Kaneko Y, Chuenchit B, Harashima S (2012) Superior thermotolerance of Saccharomyces cerevisiae for efficient bioethanol fermentation can be achieved by overexpression of RSP5 ubiquitin ligase. Biotechnol Adv 30:1289–1300
Shobayashi M, Mitsueda S, Ago M, Fujii T, Iwashita K, Iefuji H (2005) Effects of culture conditions on ergosterol biosynthesis by Saccharomyces cerevisiae. Biosci Biotechnol Biochem 69:2381–2388
Sorger PK, Pelham HR (1987) Purification and characterization of a heat-shock element binding protein from yeast. EMBO J 6:3035–3041
Sorger PK, Pelham HR (1988) Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell 54:855–864
Takahashi T, Shimoi H, Ito K (2001) Identification of genes required for growth under ethanol stress using transposon mutagenesis in Saccharomyces cerevisiae. Mol Genet Genomics 265:1112–1119
Talarek N, Cameroni E, Jaquenoud M, Luo X, Bontron S, Lippman S, Devgan G, Snyder M, Broach JR, De Virgilio C (2010) Initiation of the TORC1-regulated G0 program requires Igo1/2, which license specific mRNAs to evade degradation via the 5′-3′ mRNA decay pathway. Mol Cell 38:345–355
Tao X, Zheng D, Liu T, Wang P, Zhao W, Zhu M, Jiang X, Zhao Y, Wu X (2012) A novel strategy to construct yeast Saccharomyces cerevisiae strains for very high gravity fermentation. PLoS One 7:e31235
Treger JM, Schmitt AP, Simon JR, McEntee K (1998) Transcriptional factor mutations reveal regulatory complexities of heat shock and newly identified stress genes in Saccharomyces cerevisiae. J Biol Chem 273:26875–26879
Urbanczyk H, Noguchi C, Wu H, Watanabe D, Akao T, Takagi H, Shimoi H (2011) Sake yeast strains have difficulty in entering a quiescent state after cell growth cessation. J Biosci Bioeng 112:44–48
Varela C, Cárdenas J, Melo F, Agosin E (2005) Quantitative analysis of wine yeast gene expression profiles under winemaking conditions. Yeast 22:369–383
Walkey CJ, Luo Z, Borchers CH, Measday V, van Vuuren HJ (2011) The Saccharomyces cerevisiae fermentation stress response protein Igd1p/Yfr017p regulates glycogen levels by inhibiting the glycogen debranching enzyme. FEMS Yeast Res 11:499–508
Walkey CJ, Luo Z, Madilao LL, van Vuuren HJ (2012) The fermentation stress response protein Aaf1p/Yml081Wp regulates acetate production in Saccharomyces cerevisiae. PLoS One 7:e51551
Watanabe M, Tamura K, Magbanua JP, Takano K, Kitamoto K, Kitagaki H, Akao T, Shimoi H (2007) Elevated expression of genes under the control of stress response element (STRE) and Msn2p in an ethanol-tolerance sake yeast Kyokai no. 11. J Biosci Bioeng 104:163–170
Watanabe M, Watanabe D, Akao T, Shimoi H (2009) Overexpression of MSN2 in a sake yeast strain promotes ethanol tolerance and increases ethanol production in sake brewing. J Biosci Bioeng 107:516–518
Watanabe D, Nogami S, Ohya Y, Kanno Y, Zhou Y, Akao T, Shimoi H (2011a) Ethanol fermentation driven by elevated expression of the G1 cyclin gene CLN3 in sake yeast. J Biosci Bioeng 112:577–582
Watanabe D, Ota T, Nitta F, Akao T, Shimoi H (2011b) Automatic measurement of sake fermentation kinetics using a multi-channel gas monitor system. J Biosci Bioeng 112:54–57
Watanabe D, Wu H, Noguchi C, Zhou Y, Akao T, Shimoi H (2011c) Enhancement of the initial rate of ethanol fermentation due to dysfunction of yeast stress response components Msn2p and/or Msn4p. Appl Environ Microbiol 77:934–941
Watanabe D, Araki Y, Zhou Y, Maeya N, Akao T, Shimoi H (2012) A loss-of-function mutation in the PAS kinase Rim15p is related to defective quiescence entry and high fermentation rates of Saccharomyces cerevisiae sake yeast strains. Appl Environ Microbiol 78:4008–4016
Watanabe D, Hashimoto N, Mizuno M, Zhou Y, Akao T, Shimoi H (2013) Accelerated alcoholic fermentation caused by defective gene expression related to glucose derepression in Saccharomyces cerevisiae. Biosci Biotechnol Biochem 77:2255–2262
Wiederrecht G, Seto D, Parker CS (1988) Isolation of the gene encoding the S. cerevisiae heat shock transcription factor. Cell 54:841–853
Wu H, Zheng X, Araki Y, Sahara H, Takagi H, Shimoi H (2006) Global gene expression analysis of yeast cells during sake brewing. Appl Environ Microbiol 72:7353–7358
Wu H, Watanabe T, Araki Y, Kitagaki H, Akao T, Takagi H, Shimoi H (2009) Disruption of ubiquitin-related genes in laboratory yeast strains enhances ethanol production during sake brewing. J Biosci Bioeng 107:636–640
Xie MW, Jin F, Hwang H, Hwang S, Anand V, Duncan MC, Huang J (2005) Insights into TOR function and rapamycin response: chemical genomic profiling by using a high-density cell array method. Proc Natl Acad Sci U S A 102:7215–7220
Yamada T, Shimoi H, Ito K (2005) High expression of unsaturated fatty acid synthesis gene OLE1 in sake yeasts. J Biosci Bioeng 99:512–516
Yamaji K, Hara S, Mizoguchi H (2003) Influence of Ras function on ethanol stress response of sake yeast. J Biosci Bioeng 96:474–480
Yang J, Bae JY, Lee YM, Kwon H, Moon HY, Kang HA, Yee SB, Kim W, Choi W (2011) Construction of Saccharomyces cerevisiae strains with enhanced ethanol tolerance by mutagenesis of the TATA-binding protein gene and identification of novel genes associated with ethanol tolerance. Biotechnol Bioeng 108:1776–1787
Yoshida S, Imoto J, Minato T, Oouchi R, Sugihara M, Imai T, Ishiguro T, Mizutani S, Tomita M, Soga T, Yoshimoto H (2008) Development of bottom-fermenting Saccharomyces strains that produce high SO2 levels, using integrated metabolome and transcriptome analysis. Appl Environ Microbiol 74:2787–2796
Zuzuarregui A, del Olmo M (2004) Analyses of stress resistance under laboratory conditions constitute a suitable criterion for wine yeast selection. Antonie Van Leeuwenhoek 85:271–280
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Watanabe, D., Takagi, H., Shimoi, H. (2015). Mechanism of High Alcoholic Fermentation Ability of Sake Yeast. In: Takagi, H., Kitagaki, H. (eds) Stress Biology of Yeasts and Fungi. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55248-2_4
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